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Abstract Maternal transmission of microbes occurs across the animal kingdom and is vital for offspring development and long-term health. The mechanisms of this transfer are most well-studied in humans and other mammals but are less well-understood in egg-laying animals, especially those with no parental care. Here, we investigate the transfer of maternal microbes in the oviparous phrynosomatid lizard, Sceloporus virgatus. We compared the microbiota of three maternal tissues—oviduct, cloaca, and intestine—to three offspring sample types: egg contents and eggshells on the day of oviposition, and hatchling intestinal tissue on the day of hatching. We found that maternal identity is an important factor in hatchling microbiome composition, indicating that maternal transmission is occurring. The maternal cloacal and oviductal communities contribute to offspring microbiota in all three sample types, with minimal microbes sourced from maternal intestines. This indicates that the maternal reproductive microbiome is more important for microbial inheritance than the gut microbiome, and the tissue-level variation of the adult S. virgatus microbiota must develop as the hatchling matures. Despite differences between adult and hatchling communities, offspring microbiota were primarily members of the Enterobacteriaceae and Yersiniaceae families (Phylum Proteobacteria), consistent with this and past studies of adult S. virgatus microbiomes.
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Cloacal microbiomes of sympatric and allopatric Sceloporus lizards vary with environment and host relatedness
Animals and their microbiomes exert reciprocal influence; the host’s environment, physiology, and phylogeny can impact the composition of the microbiome, while the microbes present can affect host behavior, health, and fitness. While some microbiomes are highly malleable, specialized microbiomes that provide important functions can be more robust to environmental perturbations. Recent evidence suggests Sceloporus virgatus has one such specialized microbiome, which functions to protect eggs from fungal pathogens during incubation. Here, we examine the cloacal microbiome of three different Sceloporus species (spiny lizards; Family Phrynosomatidae)– Sceloporus virgatus , Sceloporus jarrovii , and Sceloporus occidentalis . We compare two species with different reproductive modes (oviparous vs. viviparous) living in sympatry: S . virgatus and S . jarrovii . We compare sister species living in similar habitats (riparian oak-pine woodlands) but different latitudes: S . virgatus and S . occidentalis . And, we compare three populations of one species ( S . occidentalis ) living in different habitat types: beach, low elevation forest, and the riparian woodland. We found differences in beta diversity metrics between all three comparisons, although those differences were more extreme between animals in different environments, even though those populations were more closely related. Similarly, alpha diversity varied among the S . occidentalis populations and between S . occidentalis and S . virgatus , but not between sympatric S . virgatus and S . jarrovii . Despite these differences, all three species and all three populations of S . occcidentalis had the same dominant taxon, Enterobacteriaceae . The majority of the variation between groups was in low abundance taxa and at the ASV level; these taxa are responsive to habitat differences, geographic distance, and host relatedness. Uncovering what factors influence the composition of wild microbiomes is important to understanding the ecology and evolution of the host animals, and can lead to more detailed exploration of the function of particular microbes and the community as a whole.
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- Award ID(s):
- 1755408
- PAR ID:
- 10401929
- Editor(s):
- Ruiz-Rodriguez, Magdalena
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 17
- Issue:
- 12
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0279288
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0279288
